Amyloid formation by human carboxypeptidase D transthyretin-like domain under physiological conditions

Journal of Biological Chemistry

Volumn 289, Issue 49, 2014, Pages 33783-33796

  Garcia Pardo, Javier ^a   Graña Montes, Ricardo ^a   Fernandez Mendez, Marc ^a   Ruyra, Angels ^a   Roher, Nerea ^a   Avile, Francesc X ^a   Lorenzo, Julia ^a   Ventura, Salvador ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; CONFORMATIONS; GLYCOPROTEINS; PHYSIOLOGY;

AGGREGATION PROPENSITY; BIOLOGICAL ENVIRONMENTS; CONFORMATIONAL STABILITIES; INTRINSIC PROPERTY; PHYSIOLOGICAL CONDITION; PROTEIN AGGREGATION; STRUCTURAL ELEMENTS; STRUCTURAL HOMOLOGY;

PROTEINS;

AMYLOID PROTEIN; CARBOXYPEPTIDASE D; PREALBUMIN; AMYLOID; METALLOCARBOXYPEPTIDASE D; PROTEIN; PROTEIN AGGREGATE; RECOMBINANT PROTEIN;

ARTICLE; ENZYME ACTIVITY; ENZYME STABILITY; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; PROTEIN INTERACTION; PROTEIN PURIFICATION; REGULATORY MECHANISM; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; PH; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; AMYLOID; ESCHERICHIA COLI; GENE EXPRESSION; HUMANS; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PREALBUMIN; PROTEIN AGGREGATES; PROTEIN FOLDING; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84917690463     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.594804     Document Type: Article

References (67)

1. Fernández, D., Pallarès, I., Vendrell, J., and Avilés, F. X. (2010) Progress in metallocarboxypeptidases and their small molecular weight inhibitors. Biochimie 92, 1484-1500
2. Rodriguez de la Vega, M., Sevilla, R. G., Hermoso, A., Lorenzo, J., Tanco, S., Diez, A., Fricker, L. D., Bautista, J. M., and Avilés, F. X. (2007) Nna1-like proteins are active metallocarboxypeptidases of a new and diverse M14 subfamily. FASEB J. 21, 851-865
3. Arolas, J. L., Vendrell, J., Aviles, F. X., and Fricker, L. D. (2007) Metallocarboxypeptidases: emerging drug targets in biomedicine. Curr. Pharm. Des. 13, 349-366
4. Reznik, S. E., and Fricker, L. D. (2001) Carboxypeptidases from A to Z: implications in embryonic development and Wnt binding. Cell. Mol. Life Sci. 58, 1790-1804
5. Aloy, P., Companys, V., Vendrell, J., Aviles, F. X., Fricker, L. D., Coll, M., and Gomis-Rüth, F. X. (2001) The crystal structure of the inhibitor-complexed carboxypeptidase D domain II and the modeling of regulatory carboxypeptidases. J. Biol. Chem. 276, 16177-16184
6. Gomis-Rüth, F. X., Companys, V., Qian, Y., Fricker, L. D., Vendrell, J., Avilés, F. X., and Coll, M. (1999) Crystal structure of avian carboxypeptidase D domain II: a prototype for the regulatory metallocarboxypeptidase subfamily. EMBO J. 18, 5817-5826
7. Keil, C., Maskos, K., Than, M., Hoopes, J. T., Huber, R., Tan, F., Deddish, P. A., Erdös, E. G., Skidgel, R. A., and Bode, W. (2007) Crystal structure of the human carboxypeptidase N (kininase I) catalytic domain. J. Mol. Biol. 366, 504-516
8. Reverter, D., Maskos, K., Tan, F., Skidgel, R. A., and Bode, W. (2004) Crystal structure of human carboxypeptidase M, a membrane-bound enzyme that regulates peptide hormone activity. J. Mol. Biol. 338, 257-269
9. Tanco, S., Arolas, J. L., Guevara, T., Lorenzo, J., Avilés, F. X., and Gomis- Rüth, F. X. (2010) Structure-function analysis of the short splicing variant carboxypeptidase encoded by Drosophila melanogaster silver. J. Mol. Biol. 401, 465-477
10. Sidyelyeva, G., Baker, N. E., and Fricker, L. D. (2006) Characterization of the molecular basis of the Drosophila mutations in carboxypeptidase D. Effect on enzyme activity and expression. J. Biol. Chem. 281, 13844-13852
11. Eng, F. J., Novikova, E. G., Kuroki, K., Ganem, D., and Fricker, L. D. (1998) gp180, a protein that binds duck hepatitis B virus particles, has metallocarboxypeptidase D-like enzymatic activity. J. Biol. Chem. 273, 8382-8388
12. Kuroki, K., Eng, F., Ishikawa, T., Turck, C., Harada, F., and Ganem, D. (1995) gp180, a host cell glycoprotein that binds duck hepatitis B virus particles, is encoded by a member of the carboxypeptidase gene family. J. Biol. Chem. 270, 15022-15028
13. Cornwell, G. G., 3rd, Sletten, K., Johansson, B., and Westermark, P. (1988) Evidence that the amyloid fibril protein in senile systemic amyloidosis is derived from normal prealbumin. Biochem. Biophys. Res. Commun. 154, 648-653
14. Westermark, P., Sletten, K., Johansson, B., and Cornwell, G. G., III (1990) Fibril in senile systemic amyloidosis is derived from normal transthyretin. Proc. Natl. Acad. Sci. U.S.A. 87, 2843-2845
15. Saraiva, M. J., Costa, P. P., Birken, S., and Goodman, D. S. (1983) Presence of an abnormal transthyretin (prealbumin) in Portuguese patients with familial amyloidotic polyneuropathy. Trans. Assoc. Am. Physicians 96, 261-270
16. Hou, X., Aguilar, M. I., and Small, D. H. (2007) Transthyretin and familial amyloidotic polyneuropathy. Recent progress in understanding the molecular mechanism of neurodegeneration. FEBS J. 274, 1637-1650
17. Hammarstrom, P., Jiang, X., Hurshman, A. R., Powers, E. T., and Kelly, J. W. (2002) Sequence-dependent denaturation energetics: a major determinant in amyloid disease diversity. Proc. Natl. Acad. Sci. U.S.A. 99, Suppl. 4, 16427-16432
18. Sekijima, Y., Wiseman, R. L., Matteson, J., Hammarström, P., Miller, S. R., Sawkar, A. R., Balch, W. E., and Kelly, J. W. (2005) The biological and chemical basis for tissue-selective amyloid disease. Cell 121, 73-85
19. Ferrão-Gonzales, A. D., Palmieri, L., Valory, M., Silva, J. L., Lashuel, H., Kelly, J. W., and Foguel, D. (2003) Hydration and packing are crucial to amyloidogenesis as revealed by pressure studies on transthyretin variants that either protect or worsen amyloid disease. J. Mol. Biol. 328, 963-974
20. Foss, T. R., Wiseman, R. L., and Kelly, J. W. (2005) The pathway by which the tetrameric protein transthyretin dissociates. Biochemistry 44, 15525-15533
21. Foguel, D. (2005) High pressure studies on transthyretin. Protein Pept. Lett. 12, 245-249
22. Ferreira, P., Sant'Anna, R., Sant'Anna, O., Varejão, N., Lima, C., Novis, S., Barbosa, R. V., Caldeira, C. M., Rumjanek, F. D., Ventura, S., Cruz, M. W., and Foguel, D. (2013) Structure-based analysis of A19D, a variant of transthyretin involved in familial amyloid cardiomyopathy. PLoS One 8, e82484
23. Lai, Z., Colón, W., and Kelly, J. W. (1996) The acid-mediated denaturation pathway of transthyretin yields a conformational intermediate that can self-assemble into amyloid. Biochemistry 35, 6470-6482
24. Jiang, X., Smith, C. S., Petrassi, H. M., Hammarström, P., White, J. T., Sacchettini, J. C., and Kelly, J. W. (2001) An engineered transthyretin monomer that is nonamyloidogenic, unless it is partially denatured. Biochemistry 40, 11442-11452
25. Quintas, A., Vaz, D. C., Cardoso, I., Saraiva, M. J., and Brito, R. M. (2001) Tetramer dissociation and monomer partial unfolding precedes protofibril formation in amyloidogenic transthyretin variants. J. Biol. Chem. 276, 27207-27213
26. Castillo, V., and Ventura, S. (2009) Amyloidogenic regions and interaction surfaces overlap in globular proteins related to conformational diseases. PLoS Comput. Biol. 5, e1000476
27. Pechmann, S., Levy, E. D., Tartaglia, G. G., and Vendruscolo, M. (2009) Physicochemical principles that regulate the competition between functional and dysfunctional association of proteins. Proc. Natl. Acad. Sci. U.S.A. 106, 10159-10164
28. Monsellier, E., and Chiti, F. (2007) Prevention of amyloid-like aggregation as a driving force of protein evolution. EMBO Rep. 8, 737-742
29. Levy, E. D., De, S., and Teichmann, S. A. (2012) Cellular crowding imposes global constraints on the chemistry and evolution of proteomes. Proc. Natl. Acad. Sci. U.S.A. 109, 20461-20466
30. Guijarro, J. I., Sunde, M., Jones, J. A., Campbell, I. D., and Dobson, C. M. (1998) Amyloid fibril formation by an SH3 domain. Proc. Natl. Acad. Sci. U.S.A. 95, 4224-4228
31. Castillo, V., Chiti, F., and Ventura, S. (2013) The N-terminal helix controls the transition between the soluble and amyloid states of an FF domain. PLoS One 8, e58297
32. Pallarès, I., Vendrell, J., Avilés, F. X., and Ventura, S. (2004) Amyloid fibril formation by a partially structured intermediate state of α-chymotrypsin. J. Mol. Biol. 342, 321-331
33. Chatani, E., Yagi, H., Naiki, H., and Goto, Y. (2012) Polymorphism of β2-microglobulin amyloid fibrils manifested by ultrasonication-enhanced fibril formation in trifluoroethanol. J. Biol. Chem. 287, 22827-22837
34. Sabate, R., Espargaro, A., Graña-Montes, R., Reverter, D., and Ventura, S. (2012) Native structure protects SUMO proteins from aggregation into amyloid fibrils. Biomacromolecules 13, 1916-1926
35. Fändrich, M., Fletcher, M. A., and Dobson, C. M. (2001) Amyloid fibrils from muscle myoglobin. Nature 410, 165-166
36. Invernizzi, G., Papaleo, E., Sabate, R., and Ventura, S. (2012) Protein aggregation: mechanisms and functional consequences. Int. J. Biochem. Cell Biol. 44, 1541-1554
37. Chiti, F., and Dobson, C. M. (2009) Amyloid formation by globular proteins under native conditions. Nat. Chem. Biol. 5, 15-22
38. Soldi, G., Bemporad, F., Torrassa, S., Relini, A., Ramazzotti, M., Taddei, N., and Chiti, F. (2005) Amyloid formation of a protein in the absence of initial unfolding and destabilization of the native state. Biophys. J. 89, 4234-4244
39. Zhuravlev, P. I., Reddy, G., Straub, J. E., and Thirumalai, D. (2014) Propensity to form amyloid fibrils is encoded as excitations in the free energy landscape of monomeric proteins. J. Mol. Biol. 426, 2653-2666
40. Dumoulin, M., Kumita, J. R., and Dobson, C. M. (2006) Normal and aberrant biological self-assembly: insights from studies of human lysozyme and its amyloidogenic variants. Acc. Chem. Res. 39, 603-610
41. Bemporad, F., Vannocci, T., Varela, L., Azuaga, A. I., and Chiti, F. (2008) A model for the aggregation of the acylphosphatase from Sulfolobus solfataricus in its native-like state. Biochim. Biophys. Acta 1784, 1986-1996
42. Nordlund, A., and Oliveberg, M. (2006) Folding of Cu/Zn superoxide dismutase suggests structural hotspots for gain of neurotoxic function in ALS: parallels to precursors in amyloid disease. Proc. Natl. Acad. Sci. U.S.A. 103, 10218-10223
43. Hörnberg, A., Olofsson, A., Eneqvist, T., Lundgren, E., and Sauer- Eriksson, A. E. (2004) The β-strand D of transthyretin trapped in two discrete conformations. Biochim. Biophys. Acta 1700, 93-104
44. Ye, Y., and Godzik, A. (2003) Flexible structure alignment by chaining aligned fragment pairs allowing twists. Bioinformatics 19, Suppl. 2, 246-255
45. Zhang, Y. (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9, 40
46. Cole, C., Barber, J. D., and Barton, G. J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36, W197-W201
47. Maurer-Stroh, S., Debulpaep, M., Kuemmerer, N., Lopez de la Paz, M., Martins, I. C., Reumers, J., Morris, K. L., Copland, A., Serpell, L., Serrano, L., Schymkowitz, J. W., and Rousseau, F. (2010) Exploring the sequence determinants of amyloid structure using position-specific scoring matrices. Nat. Methods 7, 237-242
48. DeLano, W. L. (2002) The PyMOL Molecular Graphics System. DeLano Scientific, San Carlos, CA
49. Hörnberg, A., Eneqvist, T., Olofsson, A., Lundgren, E., and Sauer- Eriksson, A. E. (2000) A comparative analysis of 23 structures of the amyloidogenic protein transthyretin. J. Mol. Biol. 302, 649-669
50. Hamilton, J. A., and Benson, M. D. (2001) Transthyretin: a review from a structural perspective. Cell. Mol. Life Sci. 58, 1491-1521
51. Harata, K., Haga, K., Nakamura, A., Aoyagi, M., and Yamane, K. (1996) X-ray structure of cyclodextrin glucanotransferase from alkalophilic Bacillus sp. 1011. Comparison of two independent molecules at 1.8 A resolution. Acta Crystallogr. D Biol. Crystallogr. 52, 1136-1145
52. Orville, A. M., Elango, N., Lipscomb, J. D., and Ohlendorf, D. H. (1997) Structures of competitive inhibitor complexes of protocatechuate 3,4-dioxygenase: multiple exogenous ligand binding orientations within the active site. Biochemistry 36, 10039-10051
53. Sorimachi, K., Le Gal-Coëffet, M. F., Williamson, G., Archer, D. B., and Williamson, M. P. (1997) Solution structure of the granular starch binding domain of Aspergillus niger glucoamylase bound to beta-cyclodextrin. Structure 5, 647-661
54. Bolognesi, B., Kumita, J. R., Barros, T. P., Esbjorner, E. K., Luheshi, L. M., Crowther, D. C., Wilson, M. R., Dobson, C. M., Favrin, G., and Yerbury, J. J. (2010) ANS binding reveals common features of cytotoxic amyloid species. ACS Chem. Biol. 5, 735-740
55. Ramírez-Alvarado, M., Cocco, M. J., and Regan, L. (2003) Mutations in the B1 domain of protein G that delay the onset of amyloid fibril formation in vitro. Protein Sci. 12, 567-576
56. Ventura, S., Zurdo, J., Narayanan, S., Parreño, M., Mangues, R., Reif, B., Chiti, F., Giannoni, E., Dobson, C. M., Aviles, F. X., and Serrano, L. (2004) Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case. Proc. Natl. Acad. Sci. U.S.A. 101, 7258-7263
57. Castillo, V., Graña-Montes, R., Sabate, R., and Ventura, S. (2011) Prediction of the aggregation propensity of proteins from the primary sequence: aggregation properties of proteomes. Biotechnol. J. 6, 674-685
58. Kim, Y. E., Hipp, M. S., Bracher, A., Hayer-Hartl, M., and Hartl, F. U. (2013) Molecular chaperone functions in protein folding and proteostasis. Annu. Rev. Biochem. 82, 323-355
59. Kang, Y., Zhao, D., Liang, H., Liu, B., Zhang, Y., Liu, Q., Wang, X., and Liu, Y. (2012) Structural study of TTR-52 reveals the mechanism by which a bridging molecule mediates apoptotic cell engulfment. Genes Dev. 26, 1339-1350
60. Sabaté, R., Espargaró, A., Barbosa-Barros, L., Ventura, S., and Estelrich, J. (2012) Effect of the surface charge of artificial model membranes on the aggregation of amyloid β-peptide. Biochimie 94, 1730-1738
61. Sabaté, R., Villar-Piqué, A., Espargaró, A., and Ventura, S. (2012) Temperature dependence of the aggregation kinetics of sup35 and ure2p yeast prions. Biomacromolecules 13, 474-483
62. Dobson, C. M. (2004) Principles of protein folding, misfolding and aggregation. Semin. Cell Dev. Biol. 15, 3-16
63. Knowles, T. P., Vendruscolo, M., and Dobson, C. M. (2014) The amyloid state and its association with protein misfolding diseases. Nat. Rev. Mol. Cell Biol. 15, 384-396
64. Olofsson, A., Ippel, J. H., Wijmenga, S. S., Lundgren, E., and Ohman, A. (2004) Probing solvent accessibility of transthyretin amyloid by solution NMR spectroscopy. J. Biol. Chem. 279, 5699-5707
65. Bulawa, C. E., Connelly, S., Devit, M., Wang, L., Weigel, C., Fleming, J. A., Packman, J., Powers, E. T., Wiseman, R. L., Foss, T. R., Wilson, I. A., Kelly, J. W., and Labaudinière, R. (2012) Tafamidis, a potent and selective transthyretin kinetic stabilizer that inhibits the amyloid cascade. Proc. Natl. Acad. Sci. U.S.A. 109, 9629-9634
66. De Baets, G., Reumers, J., Delgado Blanco, J., Dopazo, J., Schymkowitz, J., and Rousseau, F. (2011) An evolutionary trade-off between protein turnover rate and protein aggregation favors a higher aggregation propensity in fast degrading proteins. PLoS Comput. Biol. 7, e1002090
67. Beerten, J., Schymkowitz, J., and Rousseau, F. (2012) Aggregation prone regions and gatekeeping residues in protein sequences. Curr. Top. Med. Chem. 12, 2470-2478